The Economic Burden of Brucellosis Care in China: Socioeconomic Status Inequality

The economic burden of brucellosis care on patients can lead to significant financial strain, despite partial coverage by medical insurance. However, there is limited research on the out-of-pocket costs faced by brucellosis patients. Therefore, our study aimed to investigate the costs and out-of-pocket expenses of brucellosis care, specifically examining the varying socioeconomic status of patients in Xinjiang, China. We collected cost and demographic data from 563 respondents and their hospital bills and employed latent variable analysis to assess socioeconomic status. The majority of patients belonged to the middle and lower socioeconomic status categories (85.97%), and they were primarily farmers and herders (82.77%). The median direct cost per brucellosis episode was USD 688.65, with out-of-pocket expenses amounting to USD 391.44. These costs exceeded both the 2020 Xinjiang and national per capita health expenditures (USD 233.66 and USD 267.21, respectively). Notably, the overall medical reimbursement rate was 48.60%, and for outpatient costs, it was merely 12.82%. Despite higher out-of-pocket costs among high socioeconomic status patients, the percentage of income spent was higher (37.23%) for patients in the lower socioeconomic status group compared to other groups (16.25% and 12.96%). In conclusion, our findings highlight that brucellosis patients are predominantly from the middle and lower socioeconomic status, with high out-of-pocket expenses placing them under significant financial pressure. Moreover, there is notable inequity in economic consequences across different socioeconomic status groups. These results call for policy interventions aimed at reducing brucellosis-related poverty and promoting equitable access to care.

poverty reduction and safeguard the livelihoods of the population.
Te availability of medical insurance coverage for brucellosis diagnosis and treatment in China is limited, with varying reimbursement rates among diferent hospital levels [7].Tis, combined with the atypical presentation of brucellosis, often leads to diagnostic delays.Lower-level hospitals face challenges in diagnosing and treating the disease, resulting in the transfer of critically ill patients to higherlevel facilities [8].As a consequence, patients incur significant out-of-pocket (OOP) expenses and additional costs for travel and subsistence, particularly in underdeveloped areas of Xinjiang.Furthermore, brucellosis was not included in the list of chronic diseases at the time of the study.As a result, the outpatient costs exceeded the coverage provided by basic medical insurance in Xinjiang, forcing patients to fully bear the remaining expenses below the payment threshold.Tis adds to the fnancial burden on individual patients.Terefore, it is important to evaluate the OOP payments of brucellosis patients and assess the economic burden among hospitals and diferent economic regions in Xinjiang.Tis knowledge is crucial for optimizing the medical reimbursement policy specifc to brucellosis patients in Xinjiang, preventing them from falling into poverty as a result of the disease, and ensuring that Xinjiang maintains its progress in poverty eradication eforts.
Te impact of socioeconomic factors on health and wellbeing is substantial, leading to greater disparities and inequalities in healthcare.Lower socioeconomic status (SES), infuenced by poor living conditions and fnancial limitations, among other factors, heightens the susceptibility to brucellosis infection, comorbidities, and unfavorable treatment outcomes.Individuals with lower SES often confront economic difculties that can worsen and perpetuate a cycle of poverty [9,10].
Previous studies on brucellosis have primarily examined the overall economic losses [11,12] and the medical costs [13][14][15][16] associated with the disease.However, these studies have not specifcally addressed the OOP costs incurred by individual patients, particularly within diferent SES.As a result, the true economic burden of brucellosis on patients may have been unclear and overlooked.In light of this, the objective of this study is to investigate the costs associated with the care of brucellosis, assess the economic burden across diferent economic regions and levels of hospitals, and evaluate the fnancial implications for individuals with varying SES.

Study Design and Setting.
A cross-sectional study was conducted in seven counties in Xinjiang, China, namely, Huocheng, Atushi, Emin, Yanqi, Yizhou, Wushi, and Shufu from April to June 2021 (Figure 1).Tese counties were randomly selected in the Chinese National Notifable Disease Reporting System (NNDRS) according to their incidence of brucellosis.Te study followed the STrengthening the Reporting of OBservational studies in Epidemiology (STROBE) for cross-sectional studies guidelines (Supplementary File 2).Te study protocol was approved by the Research Ethics Review Committee of the Chinese Center for Disease Control and Prevention (Approval number: 202120), and signed informed consent was obtained from all participants prior to the investigation.For individuals under the age of 18, we obtain informed consent from their legal guardians.

Sample Size.
Te "Confdence Intervals for One Proportion" module from Power Analysis and Sample Size Software (Version 15, NCSS LLC., East Kaysville, Utah, United States) was used to perform the sample size calculation.Based on the assumption of a 20% prevalence of patients with OOP exceeding their per capita annual household income, there were a precision of 0.07, an α level of 0.05, and a 5% dropout rate.Te calculated sample size was 557.

Sampling and Participants.
A multistage random sampling method was utilized to select aged 15 years or older who had been diagnosed with brucellosis.Tese individuals had completed full treatment for a single episode and were reported in the NNDRS between January 1, 2019, and March 1, 2021, in order to fulfll the sample size criteria.Te diagnosis of brucellosis was based on the criteria outlined in the diagnosis of brucellosis (WS 269-2019) [17].
Te sampling process was performed in three steps: in step 1, seven counties/districts in Xinjiang were randomly chosen from the NNDRS.In step 2, each township within these counties/districts was assigned a unique number based on the number of cases.Systematic sampling was then used to select 3-4 townships in each county/district.In step 3, from each selected township, 20-30 patients were randomly chosen based on the order of their diagnosis date (Figure 2).
Tis study was community-based, conducted by trained interviewers, using a uniform questionnaire to interview the subjects face by face in the communities where the selected brucellosis patients lived.Te uniform questionnaire was used to gather the following information: (1) demographic and socioeconomic characteristics of the subjects such as age, sex, education, occupation, and per capita annual household income; (2) direct medical cost such as inpatient costs, outpatient costs, medical expenses covered by insurance system, and out-of-pocket costs (OOPO) associated with each brucellosis episode of care; (3) nonmedical expenses associated with transportation and accommodation.As Xinjiang has designated hospitals for brucellosis patients for appropriate treatment, normally in county or township level hospitals, and the electronic degree of these grass-roots hospitals is very high, these direct medical costs can be obtained from the Hospital Electronic Information System.Patients can be reimbursed at hospital and only need to pay the OOPP for the medical expense.
A standardized protocol was implemented to ensure consistency in interviewer training and quality control supervision throughout all survey instances.Te interviewers included 2 provincial CDC staf and 12 trained staf from the local Centers for Disease Control and Prevention.In addition, 3-5 local volunteers who were familiar with the customs and languages of the patients Each questionnaire underwent a thorough review by qualifed supervisory staf.Data management specialists checked the collected questionnaires for completeness and logical consistency.

Cost Measurement.
Direct costs can be classifed into medical costs and nonmedical costs.Medical costs primarily consist of expenses related to self-purchased medications, outpatient diagnostic and treatment services, and hospitalization during patient treatment.On the other hand, nonmedical costs encompass additional expenses such as transportation, lodging, and food.Out-of-pocket medical costs refer to the portion of medical costs that patients must pay directly after reimbursement within a single episode of care.Out-of-pocket costs can be calculated as the sum of out-of-pocket medical costs and nonmedical costs.

Measurement of Socioeconomic Status and Regional
Classifcation.SES is a key determinant of health, as it encompasses access to material, human, and social resources.Education, employment, and income are vital components of SES and can be combined to derive an SES index [18].In this research, the SES of patients was assessed using latent class analysis (LCA) based on their income, education, and occupation [19,20].Please refer to Supplementary Appendix 1 (Supplementary File 1) for further details.Journal of Tropical Medicine Seven counties/districts have been categorized into low-, middle-, and high-economic regions based on their regional GDP and the per capita disposable income of both rural and urban residents in 2020 [21].

Data Analyses.
We employed the statistical software package RX64 4.3.0 to undertake data analysis.Descriptive statistics and percentage distributions were utilized, with median and interquartile ranges (IQR) presented.All monetary values were estimated in United States dollars (USD) using a currency exchange rate of Chinese Yuan (CNY) 689.76 to USD 100 in 2020 [22].Patients were categorized into four quartiles (Q1 to Q4) based on their per capita annual household income.Categorical data were summarized as proportions, and the x 2 test was employed to assess diferences.Te Kruskal-Wallis test was used to examine variations in various costs and proportions.

Results
In total, 595 patients met the criteria for participation in the study, and of these, 580 patients successfully completed the survey.After excluding 17 patients from the analysis, a total of 563 patients were included in the fnal analysis (Figure 2).

Sociodemographic Characteristics.
Te majority of brucellosis cases in this study were male (70.52%), of working age (76.20% aged 25-59), mainly belonging to the Uyghur ethnic group (51.69%), engaged in farming (59.15%), and had less than a high school education  2 and Figure 4).

Costs of Brucellosis in Diferent Regions and Hospitals.
In regions with low-economic status, the average annual household income per person was found to be the lowest at USD 1532.42.Interestingly, these regions also faced the highest direct costs (USD 1764.97) and OOP expenses (USD 1075.74).Te burden on tertiary hospitals and their patients was particularly high, particularly with respect to medical costs (USD 1377.68) and OOP expenses (USD 1126.48),surpassing those in lower-level hospitals.Te proportion of OOP expenses for inpatient costs increased as the level of hospitals increased, but there was minimal diference in outpatient costs (Tables 3 and 4).

Discussion
Brucellosis has been demonstrated to have signifcant negative socioeconomic impacts, with the majority of losses attributed to livestock [11].Studies have shown that brucellosis impacts society economically by afecting livestock's reproductive rates, milk production, and overall health status [23].However, within the framework of "One Health," the cost assessment of brucellosis should also consider the costs associated with human diseases.Terefore, further evaluation of the overall and individual economic burdens incurred during the treatment of human brucellosis is necessary.
Tis study aimed to examine the economic impact of brucellosis on patients in Xinjiang.Te fndings revealed a substantial fnancial burden, with brucellosis patients incurring median OOP costs that exceeded both the per capita health expenditures in Xinjiang and on a national level in 2020 [24].Moreover, this economic burden was further exacerbated by socioeconomic disparities, with economically disadvantaged patients experiencing more severe fnancial strain.Tertiary hospitals and those located in low-economic regions were particularly afected by higher fnancial burdens.Notably, while the proportions of OOP costs for inpatient care varied across hospitals, no signifcant diferences were observed for outpatient care.

Costs of Brucellosis.
Te study found that the median direct costs for managing brucellosis were USD 688.65 (IQR: 333.45, 1563.54),indicating a signifcant fnancial impact associated with this infectious disease.Te median medical costs for brucellosis (USD 541.58) were higher than the nonmedical costs (USD 101.48).Tis fnding is consistent with a previous study conducted in Jingyuan, Gansu, where the median medical costs were USD 1715.81 compared to USD 268.21 for nonmedical costs [16].Additionally, the median OOP costs for brucellosis were USD 391.44 (IQR: 202.97, 939.46), which were considerably higher than the per capita healthcare expenditure in Xinjiang (USD 233.66) and China (USD 267.21) in 2020 [24].Tis indicates that residents in Xinjiang face a signifcant fnancial strain in the treatment of brucellosis.When considering previous cost analysis research on animal brucellosis, the economic impact of this disease may pose a substantial damage to the region's agricultural economy.
Te total rate of medical reimbursement in this study was 48.60%, signifcantly lower than the coordinated fund for basic medical insurance for urban and rural residents in Xinjiang at the end of 2020 (68.10%) [25].Tis discrepancy may be attributed to the lack of coverage for all outpatient treatments for human brucellosis under medical insurance in Xinjiang during the study period, resulting in a very low outpatient reimbursement rate (12.82%).Tis highlights a potential inadequacy in 6 Journal of Tropical Medicine  Xinjiang's brucellosis medical insurance policy, which could impose a heavy fnancial burden on patients who require frequent outpatient visits, particularly those with chronic conditions.Fortunately, in November 2023, the Xinjiang government added brucellosis to the list of outpatient chronic diseases covered by the basic medical insurance for the Xinjiang Uygur Autonomous Region [26].Consequently, outpatient brucellosis services will no longer have a deductible, and the reimbursement limit will be signifcantly increased.Tis important development is expected to substantially alleviate the fnancial burden on patients.

SES Inequality in Economic Consequences of Brucellosis.
Te results of our study indicate that individuals afected by brucellosis in Xinjiang are primarily from low and middle SES backgrounds.Teir median per capita annual household income was found to be below the national lower middleincome group (USD 2383.87), at USD 956.85 and USD 1742.64,respectively [27].Te majority of these individuals work as farmers or herders, and they have lower levels of education and social status.Tey also have limited sources of income, which contributes to their economic disadvantages in efectively responding to the challenges posed by brucellosis.Brucellosis is a disease associated with poverty, and it particularly afects the most economically disadvantaged individuals [28].In our study, we found that patients with higher SES had higher OOP costs compared to those with lower SES.However, when considering OOP costs as a percentage of per capita annual household income, the burden decreased with higher SES.Tese fndings are consistent with a previous study on tuberculosis patients, which showed that patients with low ability to pay and that even low-cost medical care could signifcantly impact their families [7].Terefore, socioeconomic disparities worsen the economic consequences of brucellosis, placing a greater fnancial burden on economically disadvantaged patients.

Brucellosis Economic Burden: Disparities in Regions and
Hospitals.Te healthcare burden is highest in tertiary hospitals and regions with low-economic levels, which may be attributed to the unequal distribution of healthcare resources.Regions with low income, particularly those in remote areas, often face limited access to medical resources [29].Tis lack of resources leads to higher expenses for transportation and accommodation when seeking care, resulting in discouragement and delays in seeking care.Tertiary hospitals, being equipped with better medical resources, usually handle high-risk patients requiring urgent and comprehensive care, resulting in increased medical costs.Diferences in charging policies and reimbursement limits among hospitals contribute to variations in the OOP proportions for healthcare expenses [30,31].Our study shows that primary hospitals have the lowest OOP proportions for inpatient costs, while tertiary hospitals have the highest proportions, which is consistent with current health policy trends [30].However, despite eforts to align with comprehensive health care provision, reimbursement for outpatient services remains limited even in primary and lower-level Medicare Priority Hospitals.Tis indicates challenges in expanding comprehensive healthcare beyond inpatient care.

Policy Implications
Xinjiang was found to bear a signifcant economic burden in the context of brucellosis care.Te majority of brucellosis patients in this region were from middle to lower socioeconomic status, and the high out-of-pocket expenses related to brucellosis care imposed substantial fnancial pressure on them.It is evident that the existing medical insurance policies fall short in terms of providing sufcient fnancial risk protection for these patients.Terefore, it is imperative to implement measures that aim at reducing and compensating for the medical costs borne by patients.Tis could involve lowering the deductible threshold for brucellosis treatment and expanding the coverage of outpatient services in the medical insurance program.In addition, policymakers should also address the equitable distribution of healthcare resources among regions and hospitals to ensure a fair sharing of the healthcare burden.Te government needs to improve preventive measures and enhance the diagnostic and treatment capabilities of primary hospitals to diminish the hospitalization rate among brucellosis patients.Finally, when formulating welfare and protection policies for brucellosis patients, the socioeconomic inequality should be taken into account to efectively alleviate the fnancial burden on vulnerable groups.

Study Limitations.
Te study acknowledges certain limitations that warrant consideration.Owing to the absence of standardized criteria for precisely estimating such costs, the analysis did not encompass indirect expenses linked to brucellosis patients, such as productivity losses resulting from absenteeism.Consequently, there may have been an underestimation of the economic impact of brucellosis on patients.Future studies should employ internationally standardized cost measurement methods to comprehensively assess the fnancial burden of human brucellosis.As a result, the economic burden of brucellosis on patients may have been underestimated.Future studies should employ internationally standardized cost measurement methods to comprehensively assess the fnancial burden of human brucellosis.Additionally, due to the retrospective nature of our study, recall bias was unavoidable.To minimize its infuence, we chose to concentrate on the most recent episode of brucellosis for each participant.

Conclusion
Brucellosis imposes a signifcant economic burden on both the healthcare system and afected individuals.Patients with low socioeconomic status are particularly vulnerable to the inequitable economic consequences of this disease.Targeted fnancial and social support for disadvantaged groups has been shown to efectively alleviate the economic burden experienced by brucellosis patients.Furthermore, it is recommended to optimize the health insurance structure by reducing the deductible threshold for brucellosis treatment and expanding the coverage of medical insurance services.

Figure 3 :
Figure 3: Brucellosis-related medical costs and payment components.

Figure 4 :
Figure 4: OOP (out-of-pocket) costs as a percentage of reported per capita annual household income across socioeconomic statuses (SESs).
Seven counties/districts in Xinjiang were selected randomly from the Chinese National Notifable Disease Reporting System (NNDRS).3-4 townships/towns were selected in each counties/districts by systematic sampling based on the number of cases, a total of 28 townships are extracted 20-30 patients reported with brucellosis in Legal Infectious Disease Reporting System from January 1, 2019 to March 3, 2021 were randomly selected based on the order of diagnosis date from each township A total of 595 patients with brucellosis were eligibleFrom April 1, 2021 to June 31, 2021, patients will be interviewed face to face/by phone and the hospital information system will be consulted.
A total of 580 patients completed the survey Exclusion criteria: ①Patients with incomplete information; ②People with comprehension difculties, hearing or visual impairments; A total of 17 patients were excluded ①3 patients had severe immunodefciency diseases; ②14 cases of critical information missing.3.2.Costs of BrucellosisCare.Te median direct costs for the entire brucellosis episode were USD 688.65, with an interquartile range (IQR) of 333.45 to 1563.54.Medical costs were signifcantly higher than nonmedical costs, with median values of USD 541.28 and USD 101.48, respectively.Te median out-of-pocket (OOP) costs amounted to USD 391.44, with an IQR of 202.97 to 939.46.Tese fgures were considerably higher than the per capita healthcare expenditure in Xinjiang and China in 2020, which were USD 233.66 and USD 267.21, respectively.It is worth noting that the overall reimbursement rate for medical costs was only 48.60%, and health insurance only reimbursed 12.82% of outpatient costs (Table2and Figure3).

Table 1 :
Sociodemographic and clinical characteristics of participants.

Table 1 :
Continued.Te acute stage was defned as the period within three months from onset to diagnosis, the subacute stage spans three to six months, and the chronic a Xinjiang was divided into South Xinjiang and North Xinjiang by the Tianshan Mountains.b Income quartiles were arranged from lower to higher (Q1 � d
a Currency exchange rate: CNY 689.76 to USD 100.b Te income indicator is measured by per capita annual household income.c Data from the 2020 China Health Statistics Yearbook.Abbreviations: OOP: out-of-pocket; USD: United States Dollar; SES: socioeconomic Status.* p value <0.05.

Table 3 :
Brucellosis-related costs (USD) in regions and hospitals.